Data from: The cryptic origins of evolutionary novelty: 1,000-fold-faster trophic diversification rates without increased ecological opportunity or hybrid swarm

Ecological opportunity is frequently proposed as the sole ingredient for adaptive radiation into novel niches. An additional trigger may be genome-wide hybridization resulting from ‘hybrid swarm’. However, these hypotheses have been difficult to test due to the rarity of comparable control environments lacking adaptive radiations. Here I exploit such a pattern in microendemic radiations of Caribbean pupfishes. I show that a sympatric three-species radiation on San Salvador Island, Bahamas diversified 1,445 times faster than neighboring islands in jaw length due to evolution of a novel scale-eating adaptive zone from a generalist ancestral niche. I then sampled 22 generalist populations on seven neighboring islands and measured morphological diversity, stomach content diversity, dietary isotopic diversity, genetic diversity, lake/island areas, macroalgae richness, and Caribbean-wide patterns of gene flow. None of these standard metrics of ecological opportunity or gene flow were associated with adaptive radiation, except for slight increases in macroalgae richness. Thus, exceptional trophic diversification is highly localized despite myriad generalist populations in comparable environmental and genetic backgrounds. This study provides a strong counterexample to the ecological/hybrid-swarm theories of adaptive radiation and suggests that diversification of novel specialists on a sparse fitness landscape is constrained by more than ecological opportunity and gene flow.

生态机遇（ecological opportunity）常被学界提出为驱动类群向新生态位（novel niches）发生适应辐射（adaptive radiation）的唯一核心要素。此外，由“杂交群（hybrid swarm）”引发的全基因组杂交（genome-wide hybridization），或可作为另一触发条件。然而，由于缺乏尚未发生适应辐射的可比对照环境（control environments），上述假说始终难以得到有效验证。本研究以加勒比鳉鱼（Caribbean pupfishes）的微特有辐射演化（microendemic radiations）类群为研究材料，恰好利用了这类兼具辐射类群与对照类群的研究体系。研究发现，巴哈马圣萨尔瓦多岛（San Salvador Island）上的同域三物种辐射类群（sympatric three-species radiation），其颌骨长度（jaw length）的演化速率是邻近岛屿类群的1445倍——这一差异源于泛化祖先生态位（generalist ancestral niche）类群演化出了全新的食鳞适应域（scale-eating adaptive zone）。随后，我们在7座邻近岛屿上采集了22个泛化种群样本，并对其形态多样性（morphological diversity）、胃内容物多样性（stomach content diversity）、膳食同位素多样性（dietary isotopic diversity）、遗传多样性（genetic diversity）、湖泊/岛屿面积（lake/island areas）、大型藻类丰富度（macroalgae richness）以及全加勒比区域的基因流模式（Caribbean-wide patterns of gene flow）进行了测定。除大型藻类丰富度存在小幅提升外，上述各类用于衡量生态机遇或基因流的标准指标，均未与适应辐射呈现显著关联。由此可见，尽管在环境与遗传背景可比的区域存在大量泛化种群，但异常显著的营养级分化（trophic diversification）仍呈现高度局域化特征。本研究为适应辐射的生态假说与杂交群假说提供了强有力的反例，同时表明：在稀疏适应度景观（fitness landscape）下，全新特化类群的分化过程所受的限制，不止于生态机遇与基因流两大因素。